Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway

Journal of Neuroscience

Volumn 27, Issue 22, 2007, Pages 5885-5894

  Tsokas, Panayiotis ^a   Ma, Tao ^a   Iyengar, Ravi ^a   Landau, Emmanuel M ^a,b   Blitzer, Robert D ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Dendrites; ERK; Hippocampus; LTP; Mammalian target of rapamycin; Mitogen activated protein kinase; Protein synthesis; Synaptic plasticity

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT KINASE 1; S6 KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PYRAMIDAL NERVE CELL; RAT; REGULATORY MECHANISM; STIMULATION; UPREGULATION;

ANIMALS; DENDRITES; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UP-REGULATION;

EID: 34249829585     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4548-06.2007     Document Type: Article

References (82)

1. Alarcon JM, Barco A, Kandel ER (2006) Capture of the late phase of long-term potentiation within and across the apical and basilar dendritic compartments of CA1 pyramidal neurons: synaptic tagging is compartment restricted. J Neurosci 26:256-264.
2. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P (1997a) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα-. Curr Biol 7:261-269.
3. Alessi DR, Deak M, Casamayor A, Caudwell FB, Morrice N, Norman DG, Gaffney P, Reese CB, MacDougall CN, Harbison D, Ashworth A, Bownes M (1997b) 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr Biol 7:776-789.
4. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
5. 2+/calmodulin-dependent protein kinase II and protein phosphatase 1 during hippocampal long-term potentiation. J Neurosci 25:5604-5610.
6. Banko JL, Hou L, Klann E (2004) NMDA receptor activation results in PKA- and ERK-dependent Mnk1 activation and increased eIF4E phosphorylation in hippocampal area CA1. J Neurochem 91:462-470.
7. Banko JL, Poulin F, Hou L, DeMaria CT, Sonenberg N, Klann E (2005) The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci 25:9581-9590.
8. Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689-703.
9. Biondi RM, Cheung PC, Casamayor A, Deak M, Currie RA, AlessiDR (2000) Identification of a pocket in the PDK1 kinase domain that interacts with PIF and the C-terminal residues of PKA. EMBO J 19:979-988.
10. Blitzer RD, Iyengar R, Landau EM (2005) Postsynaptic signaling networks: cellular cogwheels underlying long-term plasticity. Biol Psychiatry 57:113-119.
11. Brazil DP, Hemmings BA (2001) Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 26:657-664.
12. Cammalleri M, Lutjens R, Berton F, King AR, Simpson C, Francesconi W, Sanna PP (2003) Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc Natl Acad Sci USA 100:14368-14373.
13. Chan TO, Rittenhouse SE, Tsichlis PN (1999) AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation. Annu Rev Biochem 68:965-1014.
14. Cheng X, Ma Y, Moore M, Hemmings BA, Taylor SS (1998) Phosphorylation and activation of cAMP-dependent protein kinase by phosphoinositide-dependent protein kinase. Proc Natl Acad Sci USA 95:9849-9854.
15. Chou MM, Hou W, Johnson J, Graham LK, Lee MH, Chen CS, Newton AC, Schaffhausen BS, Toker A (1998) Regulation of protein kinase C ζ by PI 3-kinase and PDK-1. Curr Biol 8:1069-1077.
16. Cracco JB, Serrano P, Moskowitz SI, Bergold PJ, Sacktor TC (2005) Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 15:551-556.
17. Currie RA, Walker KS, Gray A, Deak M, Casamayor A, Downes CP, Cohen P, Alessi DR, Lucocq J (1999) Role of phosphatidylinositol 3,4,5-trisphosphate in regulating the activity and localization of 3-phosphoinositide-dependent protein kinase-1. Biochem J 337:575-583.
18. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J Neurosci 20:4563-4572.
19. Dummler BA, Hauge C, Silber J, Yntema HG, Kruse LS, Kofoed B, Hemmings BA, Alessi DR, Frodin M (2005) Functional characterization of human RSK4, a new 90-kDa ribosomal S6 kinase, reveals constitutive activation in most cell types. J Biol Chem 280:13304-13314.
20. Dutil EM, Toker A, Newton AC (1998) Regulation of conventional protein kinase C isozymes by phosphoinositide-dependent kinase 1 (PDK-1). Curr Biol 8:1366-1375.
21. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
22. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
23. Frey U, Morris RG (1998) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545-552.
24. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
25. Frey U, Krug M, Brodemann R, Reymann K, Matthies H (1989) Long-term potentiation induced in dendrites separated from rat's CA1 pyramidal somata does not establish a late phase. Neurosci Lett 97:135-139.
26. Frödin M, Jensen CJ, Merienne K, Gammeltoft S (2000) A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J 19:2924-2934.
27. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N (1999) Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13:1422-1437.
28. Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7:575-583.
29. Holz MK, Blenis J (2005) Identification of S6 kinase 1 as a novel mammalian target of rapamycin (mTOR)-phosphorylating kinase. J Biol Chem 280:26089-26093.
30. Hou L, Klann E (2004) Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24:6352-6361.
31. Huang YS, Jung MY, Sarkissian M, Richter JD (2002) N-methyl- D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and α-CaMKII mRNA polyadenylation at synapses. EMBO J 21:2139-2148.
32. Huang YY, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74-82.
33. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
34. Inoki K, Li Y, Zhu T, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4:648-657.
35. Ishizuka N, Cowan WM, Amaral DG (1995) A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J Comp Neurol 362:17-45.
36. s6k. EMBO J 16:3693-3704.
37. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402-1406.
38. Kelleher III RJ, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479.
39. Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:683-696.
40. Lehman JA, Calvo V, Gomez-Cambronero J (2003) Mechanism of ribosomal p70S6 kinase activation by granulocyte macrophage colonystimulating factor in neutrophils: cooperation of a MEK-related, THR421/SER424 kinase and a rapamycin-sensitive, m-TOR-related THR389 kinase. J Biol Chem 278:28130-28138.
41. Lin CH, Yeh SH, Lu KT, Leu TH, Chang WC, Gean PW (2001) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851.
42. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, Pandolfi PP (2005) Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121:179-193.
43. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC (2002) Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 10:151-162.
44. Marin P, Nastiuk KL, Daniel N, Girault JA, Czernik AJ, Glowinski J, Nairn AC, Premont J (1997) Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J Neurosci 17:3445-3454.
45. Megias M, Emri Z, Freund TF, Gulyas AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102:527-540.
46. Meyuhas O, Hornstein E (2000) Translational control of TOP mRNAs. In: Translational control of gene expression (Sonenberg N, Hershey JWB, Mathews MB, eds), pp 671-693. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
47. Mora A, Komander D, van Aalten DM, Alessi DR (2004) PDK1, the master regulator of AGC kinase signal transduction. Semin Cell Dev Biol 15:161-170.
48. Murga C, Laguinge L, Wetzker R, Cuadrado A, Gutkind JS (1998) Activation of Akt/protein kinase B by G protein-coupled receptors. A role for alpha and beta gamma subunits of heterotrimeric G proteins acting through phosphatidylinositol-3-OH kinasegamma. J Biol Chem 273:19080-19085.
49. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR (1999) Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344:427-431.
50. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23:3679-3688.
51. Osten P, Valsamis L, Harris A, Sacktor TC (1996) Protein synthesis-dependent formation of protein kinase Mζ in long-term potentiation. J Neurosci 16:2444-2451.
52. 2+/ calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J Neurosci 19:7823-7833.
53. Park J, Hill MM, Hess D, Brazil DP, Hofsteenge J, Hemmings BA (2001) Identification of tyrosine phosphorylation sites on 3-phosphoinositidedependent protein kinase-1 and their role in regulating kinase activity. J Biol Chem 276:37459-37471.
54. Patapoutian A, Reichardt LF (2001) Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
55. Peterson RT, Desai BN, Hardwick JS, Schreiber SL (1999) Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin associated protein. Proc Natl Acad Sci USA 96:4438-4442.
56. Potter CJ, Pedraza LG, Xu T (2002) Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol 4:658-665.
57. s6k. FEBS Lett 410:78-82.
58. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J (2004) Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101:13489-13494.
59. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22:3359-3365.
60. Sato S, Fujita N, Tsuruo T (2002) Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J Biol Chem 277:39360-39367.
61. Scheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptormediated control of protein synthesis at developing synapses. Nat Neurosci 3:211-216.
62. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME (2004) BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci 24:7366-7377.
63. Sekulic A, Hudson CC, Homme JL, Yin P, Otterness DM, Karnitz LM, Abraham RT (2000) Adirect linkage between the phosphoinositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res 60:3504-3513.
64. Stolovich M, Tang H, Hornstein E, Levy G, Cohen R, Bae SS, Birnbaum MJ, Meyuhas O (2002) Transduction of growth or mitogenic signals into translational activation of TOP mRNAs is fully reliant on the phosphatidylinositol 3-kinase-mediated pathway but requires neither S6K1 nor rpS6 phosphorylation. Mol Cell Biol 22:8101-8113.
65. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49-58.
66. Takei N, Kawamura M, Hara K, Yonezawa K, Nawa H (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes. J Biol Chem 276:42818-42825.
67. Takei N, Inamura N, Kawamura M, Namba H, Hara K, Yonezawa K, Nawa H (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24:9760-9769.
68. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci USA 99:467-472.
69. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25:5833-5843.
70. Vanhaesebroeck B, Alessi DR (2000) The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 346:561-576.
71. Vickers CA, Dickson KS, Wyllie DJ (2005) Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurones. J Physiol (Lond) 568:803-813.
72. Wang X, Paulin FE, Campbell LE, Gomez E, O'Brien K, Morrice N, Proud CG (2001) Eukaryotic initiation factor 2B: identification of multiple phosphorylation sites in the ε-subunit and their functions in vivo. EMBO J 20:4349-4359.
73. Wells DG, Richter JD, Fallon JR (2000) Molecular mechanisms for activityregulated protein synthesis in the synapto-dendritic compartment. Curr Opin Neurobiol 10:132-137.
74. Wells DG, Dong X, Quinlan EM, Huang YS, Bear MF, Richter JD, Fallon JR (2001) A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J Neurosci 21:9541-9548.
75. Wick MJ, Dong LQ, Riojas RA, Ramos FJ, Liu F (2000) Mechanism of phosphorylation of protein kinase B/Akt by a constitutively active 3-phosphoinositide-dependent protein kinase-1. J Biol Chem 275:40400-40406.
76. Wick MJ, Ramos FJ, Chen H, Quon MJ, Dong LQ, Liu F (2003) Mouse 3-phosphoinositide-dependent protein kinase-1 undergoes dimerization and trans-phosphorylation in the activation loop. J Biol Chem 278:42913-42919.
77. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by β-adrenergic receptors. Neuron 24:715-726.
78. Wu GY, Cline HT (1998) Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222-226.
79. Wu L, Wells D, Tay J, Mendis D, Abbott MA, Barnitt A, Quinlan E, Heynen A, Fallon JR, Richter JD (1998) CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses. Neuron 21:1129-1139.
80. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860-4868.
81. Zeniou M, Ding T, Trivier E, Hanauer A (2002) Expression analysis of RSK gene family members: the RSK2 gene, mutated in Coffin-Lowry syndrome, is prominently expressed in brain structures essential for cognitive function and learning. Hum Mol Genet 11:2929-2940.
82. Zhang Y, Dong Z, Nomura M, Zhong S, Chen N, Bode AM (2001) Signal transduction pathways involved in phosphorylation and activation of p70S6K after exposure to UVA irradiation. J Biol Chem 276:20913-20923.